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Annual Review of Physical Chemistry

Volume 66, 2015

Electron Transfer Mechanisms of DNA Repair by Photolyase

Abstract

Photolyase is a flavin photoenzyme that repairs two DNA base damage products induced by ultraviolet (UV) light: cyclobutane pyrimidine dimers and 6-4 photoproducts. With femtosecond spectroscopy and site-directed mutagenesis, investigators have recently made significant advances in our understanding of UV-damaged DNA repair, and the entire enzymatic dynamics can now be mapped out in real time. For dimer repair, six elementary steps have been characterized, including three electron transfer reactions and two bond-breaking processes, and their reaction times have been determined. A unique electron-tunneling pathway was identified, and the critical residues in modulating the repair function at the active site were determined. The dynamic synergy between the elementary reactions for maintaining high repair efficiency was elucidated, and the biological nature of the flavin active state was uncovered. For 6-4 photoproduct repair, a proton-coupled electron transfer repair mechanism has been revealed. The elucidation of electron transfer mechanisms and two repair photocycles is significant and provides a molecular basis for future practical applications, such as in rational drug design for curing skin cancer.

Keyword(s): dimer sequential splitting, electron tunneling pathway, flavin functional state, high repair efficiency, nonequilibrium ultrafast dynamics, proton-coupled electron transfer
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2015-04-01
2024-04-18
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Literature Cited

  1. Johns HE, Pearson ML, Leblanc JC, Helleiner CW. 1.  1964. The ultraviolet photochemistry of thymidylyl-(3′-5′)-thymidine. J. Mol. Biol. 9:503–24 [Google Scholar]
  2. Taylor JS. 2.  1994. Unraveling the molecular pathway from sunlight to skin cancer. Acc. Chem. Res. 27:76–82 [Google Scholar]
  3. Mitchell DL. 3.  1988. The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells. Photochem. Photobiol. 48:51–57 [Google Scholar]
  4. Brash DE. 4.  1997. Sunlight and the onset of skin cancer. Trends Genet. 13:410–14 [Google Scholar]
  5. Dulbecco R. 5.  1949. Reactivation of ultra-violet-inactivated bacteriophage by visible light. Nature 163:949–50 [Google Scholar]
  6. Todo T, Takemori H, Ryo H, Ihara M, Matsunaga T. 6.  et al. 1993. A new photoreactivating enzyme that specifically repairs ultraviolet light-induced (6-4)photoproducts. Nature 361:371–74 [Google Scholar]
  7. Sancar A. 7.  2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103:2203–37 [Google Scholar]
  8. Kim ST, Sancar A, Essenmacher C, Babcock GT. 8.  1993. Time-resolved EPR studies with DNA photolyase: excited-state FADH• abstracts an electron from Trp-306 to generate FADH−, the catalytically active form of the cofactor. Proc. Natl. Acad. Sci. USA 90:8023–27 [Google Scholar]
  9. Kavakli IH, Sancar A. 9.  2004. Analysis of the role of intraprotein electron transfer in photoreactivation by DNA photolyase in vivo. Biochemistry 43:15103–10 [Google Scholar]
  10. Selby CP, Sancar A. 10.  2012. The second chromophore in Drosophila photolyase/cryptochrome family photoreceptors. Biochemistry 51:167–71 [Google Scholar]
  11. Kiontke S, Gnau P, Haselsberger R, Batschauer A, Essen LO. 11.  2014. Structural and evolutionary aspects of antenna chromophore usage by class II photolyases. J. Biol. Chem. 289:19659–69 [Google Scholar]
  12. Essen LO. 12.  2006. Photolyases and cryptochromes: common mechanisms of DNA repair and light-driven signaling?. Curr. Opin. Struct. Biol. 16:51–59 [Google Scholar]
  13. Brettel K, Byrdin M. 13.  2010. Reaction mechanisms of DNA photolyase. Curr. Opin. Struct. Biol. 20:693–701 [Google Scholar]
  14. Mees A, Klar T, Gnau P, Hennecke U, Eker APM. 14.  et al. 2004. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306:1789–93 [Google Scholar]
  15. Kiontke S, Geisselbrecht Y, Pokorny R, Carell T, Batschauer A. 15.  et al. 2011. Crystal structures of an archaeal class II DNA photolyase and its complex with UV-damaged duplex DNA. EMBO J. 30:4437–49 [Google Scholar]
  16. Hitomi K, Arvai AS, Yamamoto J, Hitomi C, Teranishi M. 16.  et al. 2012. Eukaryotic class II cyclobutane pyrimidine dimer photolyase structure reveals basis for improved ultraviolet tolerance in plants. J. Biol. Chem. 287:12060–69 [Google Scholar]
  17. Pokorny R, Klar T, Hennecke U, Carell T, Batschauer A. 17.  et al. 2008. Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proc. Natl. Acad. Sci. USA 105:21023–27 [Google Scholar]
  18. Glas AF, Maul MJ, Cryle M, Barends TRM, Schneider S. 18.  et al. 2009. The archaeal cofactor F0 is a light-harvesting antenna chromophore in eukaryotes. Proc. Natl. Acad. Sci. USA 106:11540–45 [Google Scholar]
  19. Maul MJ, Barends TRM, Glas AF, Cryle MJ, Domratcheva T. 19.  et al. 2008. Crystal structure and mechanism of a DNA (6-4) photolyase. Angew. Chem. Int. Ed. Engl. 47:10076–80 [Google Scholar]
  20. Park HW, Kim ST, Sancar A, Deisenhofer J. 20.  1995. Crystal structure of DNA photolyase from Escherichia coli. Science 268:1866–72 [Google Scholar]
  21. Antony J, Medvedev DM, Stuchebrukhov AA. 21.  2000. Theoretical study of electron transfer between the photolyase catalytic cofactor FADH− and DNA thymine dimer. J. Am. Chem. Soc. 122:1057–65 [Google Scholar]
  22. Sancar A. 22.  1994. Structure and function of DNA photolyase. Biochemistry 33:2–9 [Google Scholar]
  23. Carell T, Burgdorf LT, Kundu LM, Cichon M. 23.  2001. The mechanism of action of DNA photolyases. Curr. Opin. Chem. Biol. 5:491–98 [Google Scholar]
  24. Langenbacher T, Zhao XD, Bieser G, Heelis PF, Sancar A. 24.  et al. 1997. Substrate and temperature dependence of DNA photolyase repair activity examined with ultrafast spectroscopy. J. Am. Chem. Soc. 119:10532–36 [Google Scholar]
  25. MacFarlane AW, Stanley RJ. 25.  2003. Cis-syn thymidine dimer repair by DNA photolyase in real time. Biochemistry 42:8558–68 [Google Scholar]
  26. Zhao XD, Liu JQ, Hsu DS, Zhao SY, Taylor JS. 26.  et al. 1997. Reaction mechanism of (6-4) photolyase. J. Biol. Chem. 272:32580–90 [Google Scholar]
  27. Hitomi K, Nakamura H, Kim ST, Mizukoshi T, Ishikawa T. 27.  et al. 2001. Role of two histidines in the (6-4) photolyase reaction. J. Biol. Chem. 276:10103–9 [Google Scholar]
  28. Yamamoto J, Hitomi K, Hayashi R, Getzoff ED, Iwai S. 28.  2009. Role of the carbonyl group of the (6-4) photoproduct in the (6-4) photolyase reaction. Biochemistry 48:9306–12 [Google Scholar]
  29. Schleicher E, Hitomi K, Kay CWM, Getzoff ED, Todo T. 29.  et al. 2007. Electron nuclear double resonance differentiates complementary roles for active site histidines in (6-4) photolyase. J. Biol. Chem. 282:4738–47 [Google Scholar]
  30. Kao Y-T, Saxena C, Wang L, Sancar A, Zhong D. 30.  2005. Direct observation of thymine dimer repair in DNA by photolyase. Proc. Natl. Acad. Sci. USA 102:16128–32 [Google Scholar]
  31. Kao Y-T, Saxena C, Wang L, Sancar A, Zhong D. 31.  2007. Femtochemistry in enzyme catalysis: DNA photolyase. Cell Biochem. Biophys. 48:32–44 [Google Scholar]
  32. Zhong D. 32.  2007. Ultrafast catalytic processes in enzymes. Curr. Opin. Chem. Biol. 11:174–81 [Google Scholar]
  33. Kao Y-T, Tan C, Song SH, Ozturk N, Li J. 33.  et al. 2008. Ultrafast dynamics and anionic active states of the flavin cofactor in cryptochrome and photolyase. J. Am. Chem. Soc. 130:7695–701 [Google Scholar]
  34. Liu Z, Tan C, Guo X, Kao Y-T, Li J. 34.  et al. 2011. Dynamics and mechanism of cyclobutane pyrimidine dimer repair by DNA photolyase. Proc. Natl. Acad. Sci. USA 108:14831–36 [Google Scholar]
  35. Thiagarajan V, Byrdin M, Eker APM, Muller P, Brettel K. 35.  2011. Kinetics of cyclobutane thymine dimer splitting by DNA photolyase directly monitored in the UV. Proc. Natl. Acad. Sci. USA 108:9402–7 [Google Scholar]
  36. Liu Z, Guo X, Tan C, Li J, Kao Y-T. 36.  et al. 2012. Electron tunneling pathways and role of adenine in repair of cyclobutane pyrimidine dimer by DNA photolyase. J. Am. Chem. Soc. 134:8104–14 [Google Scholar]
  37. Liu Z, Zhang M, Guo X, Tan C, Li J. 37.  et al. 2013. Dynamic determination of the functional state in photolyase and the implication for cryptochrome. Proc. Natl. Acad. Sci. USA 110:12972–77 [Google Scholar]
  38. Li J, Liu Z, Tan C, Guo X, Wang L. 38.  et al. 2010. Dynamics and mechanism of repair of ultraviolet-induced (6-4) photoproduct by photolyase. Nature 466:887–90 [Google Scholar]
  39. Tan C, Liu Z, Li J, Guo X, Wang L. 39.  et al. 2014. Molecular origin of high DNA-repair efficiency by photolyase. Manuscript in review
  40. Masson F, Laino T, Rothlisberger U, Hutter J. 40.  2009. A QM/MM investigation of thymine dimer radical anion splitting catalyzed by DNA photolyase. ChemPhysChem 10:400–10 [Google Scholar]
  41. Borg OA, Eriksson LA, Durbeej B. 41.  2007. Electron-transfer induced repair of 6-4 photoproducts in DNA: a computational study. J. Phys. Chem. A 111:2351–61 [Google Scholar]
  42. Domratcheva T, Schlichting I. 42.  2009. Electronic structure of (6-4) DNA photoproduct repair involving a non-oxetane pathway. J. Am. Chem. Soc. 131:17793–99 [Google Scholar]
  43. Sadeghian K, Bocola M, Merz T, Schutz M. 43.  2010. Theoretical study on the repair mechanism of the (6-4) photolesion by the (6-4) photolyase. J. Am. Chem. Soc. 132:16285–95 [Google Scholar]
  44. Faraji S, Dreuw A. 44.  2012. Proton-transfer-steered mechanism of photolesion repair by (6-4)-photolyases. J. Phys. Chem. Lett. 3:227–30 [Google Scholar]
  45. Harrison CB, O'Neil LL, Wiest O. 45.  2005. Computational studies of DNA photolyase. J. Phys. Chem. A 109:7001–12 [Google Scholar]
  46. Faraji S, Dreuw A. 46.  2014. Physicochemical mechanism of light-driven DNA repair by (6-4) photolyases. Annu. Rev. Phys. Chem. 65:275–92 [Google Scholar]
  47. Ueda T, Kato A, Kuramitsu S, Terasawa H, Shimada I. 47.  2005. Identification and characterization of a second chromophore of DNA photolyase from Thermus thermophilus HB27. J. Biol. Chem. 280:36237–43 [Google Scholar]
  48. Fujihashi M, Numoto N, Kobayashi Y, Mizushima A, Tsujimura M. 48.  et al. 2007. Crystal structure of archaeal photolyase from Sulfolobus tokodaii with two FAD molecules: implication of a novel light-harvesting cofactor. J. Mol. Biol. 365:903–10 [Google Scholar]
  49. Kim ST, Heelis PF, Okamura T, Hirata Y, Mataga N. 49.  et al. 1991. Determination of rates and yields of interchromophore (folate → flavin) energy transfer and intermolecular (flavin → DNA) electron transfer in Escherichia coli photolyase by time-resolved fluorescence and absorption spectroscopy. Biochemistry 30:11262–70 [Google Scholar]
  50. Jorns MS, Wang BY, Jordan SP, Chanderkar LP. 50.  1990. Chromophore function and interaction in Escherichia coli DNA photolyase: reconstitution of the apoenzyme with pterin and/or flavin derivatives. Biochemistry 29:552–61 [Google Scholar]
  51. Saxena C, Sancar A, Zhong D. 51.  2004. Femtosecond dynamics of DNA photolyase: energy transfer of antenna initiation and electron transfer of cofactor reduction. J. Phys. Chem. B 108:18026–33 [Google Scholar]
  52. Tan C, Guo L, Ai Y, Li J, Wang L. 52.  et al. 2014. Direct determination of resonance energy transfer in photolyase: structural alignment for the functional state. J. Phys. Chem. A 118:10522–30 [Google Scholar]
  53. Harbach PHP, Schneider M, Faraji S, Dreuw A. 53.  2013. Intermolecular coulombic decay in biology: the initial electron detachment from FADH− in DNA photolyases. J. Phys. Chem. Lett. 4:943–49 [Google Scholar]
  54. Stevens JA, Link JJ, Zang C, Wang L, Zhong D. 54.  2012. Ultrafast dynamics of nonequilibrium resonance energy transfer and probing globular protein flexibility of myoglobin. J. Phys. Chem. A 116:2610–19 [Google Scholar]
  55. Chang C-W, Guo L, Kao Y-T, Li J, Tan C. 55.  et al. 2010. Ultrafast solvation dynamics at binding and active sites of photolyases. Proc. Natl. Acad. Sci. USA 107:2914–19 [Google Scholar]
  56. Zheng XH, Garcia J, Stuchebrukhov AA. 56.  2008. Theoretical study of excitation energy transfer in DNA photolyase. J. Phys. Chem. B 112:8724–29 [Google Scholar]
  57. Tamada T, Kitadokoro K, Higuchi Y, Inaka K, Yasui A. 57.  et al. 1997. Crystal structure of DNA photolyase from Anacystis nidulans. Nat. Struct. Biol. 4:887–91 [Google Scholar]
  58. Aubert C, Vos MH, Mathis P, Eker APM, Brettel K. 58.  2000. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405:586–90 [Google Scholar]
  59. Byrdin M, Eker APM, Vos MH, Brettel K. 59.  2003. Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation. Proc. Natl. Acad. Sci. USA 100:8676–81 [Google Scholar]
  60. Byrdin M, Lukacs A, Thiagarajan V, Eker APM, Brettel K. 60.  et al. 2010. Quantum yield measurements of short-lived photoactivation intermediates in DNA photolyase: toward a detailed understanding of the triple tryptophan electron transfer chain. J. Phys. Chem. A 114:3207–14 [Google Scholar]
  61. Wang H, Saxena C, Quan D, Sancar A, Zhong D. 61.  2005. Femtosecond dynamics of flavin cofactor in DNA photolyase: radical reduction, local solvation, and charge recombination. J. Phys. Chem. B 109:1329–33 [Google Scholar]
  62. Liu Z, Tan C, Guo X, Li J, Wang L. 62.  et al. 2014. Dynamic determination of active-site reactivity in semiquinone photolyase by the cofactor photoreduction. J. Phys. Chem. Lett. 5:820–25 [Google Scholar]
  63. Liu Z, Tan C, Guo X, Li J, Wang L. 63.  et al. 2013. Determining complete electron flow in the cofactor photoreduction of oxidized photolyase. Proc. Natl. Acad. Sci. USA 110:12966–71 [Google Scholar]
  64. Brazard J, Usman A, Lacombat F, Ley C, Martin MM. 64.  et al. 2010. Spectro-temporal characterization of the photoactivation mechanism of two new oxidized cryptochrome/photolyase photoreceptors. J. Am. Chem. Soc. 132:4935–45 [Google Scholar]
  65. Song SH, Ozturk N, Denaro TR, Arat NO, Kao Y-T. 65.  et al. 2007. Formation and function of flavin anion radical in cryptochrome 1 blue-light photoreceptor of monarch butterfly. J. Biol. Chem. 282:17608–12 [Google Scholar]
  66. Rodgers CT, Hore PJ. 66.  2009. Chemical magnetoreception in birds: the radical pair mechanism. Proc. Natl. Acad. Sci. USA 106:353–60 [Google Scholar]
  67. Ozturk N, Selby CP, Annayev Y, Zhong D, Sancar A. 67.  2011. Reaction mechanism of Drosophila cryptochrome. Proc. Natl. Acad. Sci. USA 108:516–21 [Google Scholar]
  68. Ozturk N, Song SH, Ozgur S, Selby CP, Morrison L. 68.  et al. 2007. Structure and function of animal cryptochromes. Cold Spring Harb. Symp. Quant. Biol. 72:119–31 [Google Scholar]
  69. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T. 69.  et al. 2011. The cryptochromes: blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62:335–64 [Google Scholar]
  70. Li X, Wang Q, Yu X, Liu H, Yang H. 70.  et al. 2011. Arabidopsis cryptochrome 2 (CRY2) functions by the photoactivation mechanism distinct from the tryptophan (trp) triad-dependent photoreduction. Proc. Natl. Acad. Sci. USA 108:20844–49 [Google Scholar]
  71. Liu B, Liu HT, Zhong D, Lin C. 71.  2010. Searching for a photocycle of the cryptochrome photoreceptors. Curr. Opin. Plant Biol. 13:578–86 [Google Scholar]
  72. Brautigam CA, Smith BS, Ma ZQ, Palnitkar M, Tomchick DR. 72.  et al. 2004. Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 101:12142–47 [Google Scholar]
  73. Levy C, Zoltowski BD, Jones AR, Vaidya AT, Top D. 73.  et al. 2013. Updated structure of Drosophila cryptochrome. Nature 495:E3–4 [Google Scholar]
  74. Schmalen I, Reischl S, Wallach T, Klemz R, Grudziecki A. 74.  et al. 2014. Interaction of circadian clock proteins CRY1 and PER2 is modulated by zinc binding and disulfide bond formation. Cell 157:1203–15 [Google Scholar]
  75. Sumi H, Marcus RA. 75.  1986. Dynamic effects in electron transfer reactions. J. Chem. Phys. 84:4894–914 [Google Scholar]
  76. Wang H, Lin S, Allen JP, Williams JC, Blankert S. 76.  et al. 2007. Protein dynamics control the kinetics of initial electron transfer in photosynthesis. Science 316:747–50 [Google Scholar]
  77. Zhang L, Wang L, Kao Y-T, Qiu W, Yang Y. 77.  et al. 2007. Mapping hydration dynamics around a protein surface. Proc. Natl. Acad. Sci. USA 104:18461–66 [Google Scholar]
  78. Zhang L, Yang Y, Kao Y-T, Wang L, Zhong D. 78.  2009. Protein hydration dynamics and molecular mechanism of coupled water-protein fluctuations. J. Am. Chem. Soc. 131:10677–91 [Google Scholar]
  79. Zhong D. 79.  2009. Hydration dynamics and coupled water-protein fluctuations probed by intrinsic tryptophan. Adv. Chem. Phys. 143:83–149 [Google Scholar]
  80. Zhong D, Pal SK, Zewail AH. 80.  2011. Biological water: a critique. Chem. Phys. Lett. 503:1–11 [Google Scholar]
  81. Qin Y, Yang Y, Zhang L, Fowler JD, Qiu W. 81.  et al. 2013. Direct probing of solvent accessibility and mobility at the binding interface of polymerase (Dpo4)-DNA complex. J. Phys. Chem. A 117:13926–34 [Google Scholar]
  82. Chang C-W, He T-F, Guo L, Stevens JA, Li T. 82.  et al. 2010. Mapping solvation dynamics at the functional site of flavodoxin in three redox states. J. Am. Chem. Soc. 132:12741–47 [Google Scholar]
  83. Barbara PF, Meyer TJ, Ratner MA. 83.  1996. Contemporary issues in electron transfer research. J. Phys. Chem. 100:13148–68 [Google Scholar]
  84. Nagasawa Y, Yartsev AP, Tominaga K, Bisht PB, Johnson AE, Yoshihara K. 84.  1995. Dynamical aspects of ultrafast intermolecular electron transfer faster than solvation process: substituent effects and energy gap dependence. J. Phys. Chem. 99:653–62 [Google Scholar]
  85. LeBard DN, Kapko V, Matyushov DV. 85.  2008. Energetics and kinetics of primary charge separation in bacterial photosynthesis. J. Phys. Chem. B 112:10322–42 [Google Scholar]
  86. He T-F, Guo L, Guo X, Chang C-W, Wang L. 86.  et al. 2013. Femtosecond dynamics of short-range protein electron transfer in flavodoxin. Biochemistry 52:9120–28 [Google Scholar]
  87. Jorns MS, Sancar GB, Sancar A. 87.  1985. Identification of oligothymidylates as new simple substrates for Escherichia coli DNA photolyase and their use in a rapid spectrophotometric enzyme assay. Biochemistry 24:1856–61 [Google Scholar]
  88. Hassanali AA, Zhong D, Singer SJ. 88.  2011. An AIMD study of the CPD repair mechanism in water: reaction free energy surface and mechanistic implications. J. Phys. Chem. B 115:3848–59 [Google Scholar]
  89. Hassanali AA, Zhong D, Singer SJ. 89.  2011. An AIMD study of CPD repair mechanism in water: role of solvent in ring splitting. J. Phys. Chem. B 115:3860–71 [Google Scholar]
  90. Shih C, Museth AK, Abrahamsson M, Blanco-Rodriguez AM, Di Bilio AJ. 90.  et al. 2008. Tryptophan-accelerated electron flow through proteins. Science 320:1760–62 [Google Scholar]
  91. Stubbe J, Nocera DG, Yee CS, Chang MCY. 91.  2003. Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer?. Chem. Rev. 103:2167–201 [Google Scholar]
  92. Prytkova TR, Kurnikov IV, Beratan DN. 92.  2007. Coupling coherence distinguishes structure sensitivity in protein electron transfer. Science 315:622–25 [Google Scholar]
  93. Medvedev D, Stuchebrukhov AA. 93.  2001. DNA repair mechanism by photolyase: electron transfer path from the photolyase catalytic cofactor FADH− to DNA thymine dimer. J. Theor. Biol. 210:237–48 [Google Scholar]
  94. Prytkova TR, Beratan DN, Skourtis SS. 94.  2007. Photoselected electron transfer pathways in DNA photolyase. Proc. Natl. Acad. Sci. USA 104:802–7 [Google Scholar]
  95. Acocella A, Jones GA, Zerbetto F. 95.  2010. What is adenine doing in photolyase?. J. Phys. Chem. B 114:4101–6 [Google Scholar]
  96. Wang H, Chen X, Fang W. 96.  2014. Excited-state proton coupled electron transfer between photolyase and the damaged DNA through water wire: a photo-repair mechanism. Phys. Chem. Chem. Phys. 16:25432–41 [Google Scholar]
  97. Zhong D, Sancar A, Stuchebrukhov A. 97.  2012. Reply to Brettel and Byrdin: on the efficiency of DNA repair by photolyase. Proc. Natl. Acad. Sci. USA 109:E1463 [Google Scholar]
  98. Kao Y-T, Saxena C, He T-F, Guo L, Wang L. 98.  et al. 2008. Ultrafast dynamics of flavins in five redox states. J. Am. Chem. Soc. 130:13132–39 [Google Scholar]
  99. Moonen CTW, Vervoort J, Muller F. 99.  1984. Reinvestigation of the structure of oxidized and reduced flavin: carbon-13 and nitrogen-15 nuclear magnetic resonance study. Biochemistry 23:4859–67 [Google Scholar]
  100. Zheng Y-J, Ornstein RL. 100.  1996. A theoretical study of the structures of flavin in different oxidation and protonation states. J. Am. Chem. Soc. 118:9402–8 [Google Scholar]
  101. Huels MA, Boudaiffa B, Cloutier P, Hunting D, Sanche L. 101.  2003. Single, double, and multiple double strand breaks induced in DNA by 3–100 eV electrons. J. Am. Chem. Soc. 125:4467–77 [Google Scholar]
  102. Kim ST, Hartman RF, Rose SD. 102.  1990. Solvent dependence of pyrimidine dimer splitting in a covalently linked dimer-indole system. Photochem. Photobiol. 52:789–94 [Google Scholar]
  103. Tang WJ, Guo QX, Song Q-H. 103.  2009. Origin of solvent dependence of photosensitized splitting of a cyclobutane pyrimidine dimer by a covalently linked chromophore. J. Phys. Chem. B 113:7205–10 [Google Scholar]
  104. Kao Y-T, Song Q-H, Saxena C, Wang L, Zhong D. 104.  2012. Dynamics and mechanism of DNA repair in a biomimetic system: flavin-thymine dimer adduct. J. Am. Chem. Soc. 134:1501–3 [Google Scholar]
  105. Kim ST, Li YF, Sancar A. 105.  1992. The third chromophore of DNA photolyase: Trp-277 of Escherichia coli DNA photolyase repairs thymine dimers by direct electron transfer. Proc. Natl. Acad. Sci. USA 89:900–4 [Google Scholar]
  106. Vicic DA, Odom DT, Núñez ME, Gianolio DA, McLaughlin LW. 106.  et al. 2000. Oxidative repair of a thymine dimer in DNA from a distance by a covalently linked organic intercalator. J. Am. Chem. Soc. 122:8603–11 [Google Scholar]
  107. Yamamoto J, Martin R, Iwai S, Plaza P, Brettel K. 107.  2013. Repair of the (6-4) photoproduct by DNA photolyase requires two photons. Angew. Chem. Int. Ed. Engl. 52:7432–36 [Google Scholar]
  108. Yamamoto J, Tanaka Y, Iwai S. 108.  2009. Spectroscopic analysis of the pyrimidine(6-4)pyrimidone photoproduct: insights into the (6-4) photolyase reaction. Org. Biomol. Chem. 7:161–66 [Google Scholar]
  109. Glas AF, Schneider S, Maul MJ, Hennecke U, Carell T. 109.  2009. Crystal structure of the T(6-4)C lesion in complex with a (6-4) DNA photolyase and repair of UV-induced (6-4) and Dewar photolesions. Chem. Eur. J. 15:10387–96 [Google Scholar]
  110. Guo X, Liu Z, Song Q, Wang L, Zhong D. 110.  2015. Dynamics and mechanism of UV-damaged DNA repair in indole-thymine dimer adduct: molecular origin of low repair quantum efficiency. J. Phys. Chem. B 1193446–55
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Electron Transfer Mechanisms of DNA Repair by Photolyase
Annual Review of Physical Chemistry 66, 691 (2015); https://doi.org/10.1146/annurev-physchem-040513-103631
/content/journals/10.1146/annurev-physchem-040513-103631
/content/journals/10.1146/annurev-physchem-040513-103631
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